Publications by authors named "Colette Broekgaarden"

23 Publications

  • Page 1 of 1

SLI1 confers broad-spectrum resistance to phloem-feeding insects.

Plant Cell Environ 2021 Apr 10. Epub 2021 Apr 10.

Laboratory of Entomology, Wageningen University & Research, Wageningen, The Netherlands.

Resistance (R) genes usually compete in a coevolutionary arms race with reciprocal effectors to confer strain-specific resistance to pathogens or herbivorous insects. Here, we investigate the specificity of SLI1, a recently identified R gene in Arabidopsis that encodes a small heat shock-like protein involved in resistance to Myzus persicae aphids. In a panel with several aphid and whitefly species, SLI1 compromised reproductive rates of three species: the tobacco aphid M. persicae nicotianae, the cabbage aphid Brevicoryne brassicae and the cabbage whitefly Aleyrodes proletella. Electrical penetration graph recording of aphid behaviour, revealed shorter salivations and a 3-to-5-fold increase in phloem feeding on sli1 loss-of-function plants. The mustard aphid Lipaphis erysimi and Bemisia tabaci whitefly were not affected by SLI1. Unlike the other two aphid species, L. erysimi exhibited repetitive salivations preceding successful phloem feeding, indicating a role of salivary effectors in overcoming SLI1-mediated resistance. Microscopic characterization showed that SLI1 proteins localize in the sieve tubes of virtually all above- and below-ground tissues and co-localize with the aphid stylet tip after penetration of the sieve element plasma membrane. These observations reveal an unconventional R gene that escapes the paradigm of strain specificity and confers broad-spectrum quantitative resistance to phloem-feeding insects.
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http://dx.doi.org/10.1111/pce.14064DOI Listing
April 2021

Bioassays to Evaluate the Resistance of Whole Plants to the Herbivorous Insect Thrips.

Methods Mol Biol 2020 ;2085:93-108

Plant-Microbe Interactions, Department of Biology, Faculty of Science, Utrecht University, Utrecht, The Netherlands.

Thrips are tiny, cell-content-feeding insects that are a major pest on crops and ornamentals. Besides causing direct feeding damage, thrips may also cause indirect damage by vectoring tospoviruses. Novel resistance mechanisms to thrips need to be discovered and validated. Induction of jasmonic acid-dependent defenses has been demonstrated to be essential for resistance to thrips, but underlying mechanisms still need to be discovered. For this, it is vital to use robust plant-thrips assays to analyze plant defense responses and thrips performance. In recently developed high-throughput phenotyping platforms, the feeding damage that is visible as silver spots, and the preference of thrips in a two-choice setup is assessed, using leaf discs. Here, we describe whole-plant thrips assays that are essential for (1) validation of findings obtained by the leaf disc assays, (2) assessment of longer-term effects on thrips feeding success and fecundity, (3) determination of spatial-temporal effects induced by primary thrips infestation on a secondary attack by thrips or other insects or pathogens, and (4) assessment of gene expression and metabolite changes. We present detailed methods and tips and tricks for (a) rearing and selection of thrips at different developmental stages, (b) treatment of the whole plant or an individual leaf with thrips, and (c) determination of feeding damage and visualization of thrips oviposition success in leaves.
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http://dx.doi.org/10.1007/978-1-0716-0142-6_7DOI Listing
December 2020

Combining QTL mapping with transcriptome and metabolome profiling reveals a possible role for ABA signaling in resistance against the cabbage whitefly in cabbage.

PLoS One 2018 6;13(11):e0206103. Epub 2018 Nov 6.

Plant-Microbe Interactions, Department of Biology, Science4Life, Utrecht University, Utrecht, the Netherlands.

Whiteflies are among the world's most significant agricultural pests and chemical insecticides are extensively used to reduce crop damage to acceptable levels. However, nearly all insecticides pose a threat to the environment and alternative control methods, such as breeding of crop varieties that are inherently insect-resistant, are needed. Previously, a strong source of plant-age dependent resistance to the cabbage whitefly (Aleyrodes proletella) has been identified in the modern white cabbage (Brassica oleracea var. capitata) variety Rivera. However, nothing is known about the molecular mechanisms or the genes involved in this resistance. In the present study, a multidisciplinary approach combining transcriptome and metabolome profiling with genetic mapping was used to identify the molecular players of whitefly resistance in cabbage. Transcriptome profiles of young (susceptible) and older (resistant) Rivera plants were analyzed using RNA sequencing. While many genes involved in general processes were differentially expressed between both ages, several defense-related processes were overrepresented in the transcriptome profile of older plants. Hormone measurements revealed that jasmonic acid (JA) levels decreased upon whitefly infestation at both plant ages. Interestingly, abscisic acid (ABA) levels showed contrasting effects in response to whitefly infestation: ABA levels were reduced in young plants but induced in older plants upon whitefly feeding. Auxin levels were significantly lower in older plants compared with young plants, independent of whitefly presence, while glucosinolate levels were higher. Additionally, whitefly performance was monitored in an F2 population derived from a cross between Rivera and the susceptible white cabbage variety Christmas Drumhead. Significant QTL intervals were mapped on chromosome 2 and 9 for oviposition rate and whitefly adult survival, respectively. Several genes that were higher expressed in older plants and located in the identified QTL intervals were orthologous to Arabidopsis genes that have been related to ABA signaling, suggesting a role for ABA in the regulation of resistance towards whiteflies. Our results show that combining different omics approaches is a useful strategy to identify candidate genes underlying insect resistance.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0206103PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6219772PMC
April 2019

Thrips advisor: exploiting thrips-induced defences to combat pests on crops.

J Exp Bot 2018 04;69(8):1837-1848

Plant-Microbe Interactions, Department of Biology, Faculty of Science, Utrecht University, , TB Utrecht, The Netherlands.

Plants have developed diverse defence mechanisms to ward off herbivorous pests. However, agriculture still faces estimated crop yield losses ranging from 25% to 40% annually. These losses arise not only because of direct feeding damage, but also because many pests serve as vectors of plant viruses. Herbivorous thrips (Thysanoptera) are important pests of vegetable and ornamental crops worldwide, and encompass virtually all general problems of pests: they are highly polyphagous, hard to control because of their complex lifestyle, and they are vectors of destructive viruses. Currently, control management of thrips mainly relies on the use of chemical pesticides. However, thrips rapidly develop resistance to these pesticides. With the rising demand for more sustainable, safer, and healthier food production systems, we urgently need to pinpoint the gaps in knowledge of plant defences against thrips to enable the future development of novel control methods. In this review, we summarize the current, rather scarce, knowledge of thrips-induced plant responses and the role of phytohormonal signalling and chemical defences in these responses. We describe concrete opportunities for breeding resistance against pests such as thrips as a prototype approach for next-generation resistance breeding.
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http://dx.doi.org/10.1093/jxb/ery060DOI Listing
April 2018

Induced plant defences in biological control of arthropod pests: a double-edged sword.

Pest Manag Sci 2017 Sep 8;73(9):1780-1788. Epub 2017 Jun 8.

German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany.

Biological control is an important ecosystem service delivered by natural enemies. Together with breeding for plant defence, it constitutes one of the most promising alternatives to pesticides for controlling herbivores in sustainable crop production. Especially induced plant defences may be promising targets in plant breeding for resistance against arthropod pests. Because they are activated upon herbivore damage, costs are only incurred when defence is needed. Moreover, they can be more specific than constitutive defences. Nevertheless, inducible defence traits that are harming plant pest organisms may interfere with biological control agents, such as predators and parasitoids. Despite the vast fundamental knowledge on plant defence mechanisms and their effects on natural enemies, our understanding of the feasibility of combining biological control with induced plant defence in practice is relatively poor. In this review, we focus on arthropod pest control and present the most important features of biological control with natural enemies and of induced plant defence. Furthermore, we show potential synergies and conflicts among them and, finally, identify gaps and list opportunities for their combined use in crop protection. We suggest that breeders should focus on inducible resistance traits that are compatible with the natural enemies of arthropod pests, specifically traits that help communities of natural enemies to build up. © 2017 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.
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http://dx.doi.org/10.1002/ps.4587DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5575458PMC
September 2017

Brevicoryne brassicae aphids interfere with transcriptome responses of Arabidopsis thaliana to feeding by Plutella xylostella caterpillars in a density-dependent manner.

Oecologia 2017 Jan 22;183(1):107-120. Epub 2016 Oct 22.

Laboratory of Entomology, Wageningen University, P.O. Box 16, 6700 AA, Wageningen, The Netherlands.

Plants are commonly attacked by multiple herbivorous species. Yet, little is known about transcriptional patterns underlying plant responses to multiple insect attackers feeding simultaneously. Here, we assessed transcriptomic responses of Arabidopsis thaliana plants to simultaneous feeding by Plutella xylostella caterpillars and Brevicoryne brassicae aphids in comparison to plants infested by P. xylostella caterpillars alone, using microarray analysis. We particularly investigated how aphid feeding interferes with the transcriptomic response to P. xylostella caterpillars and whether this interference is dependent on aphid density and time since aphid attack. Various JA-responsive genes were up-regulated in response to feeding by P. xylostella caterpillars. The additional presence of aphids, both at low and high densities, clearly affected the transcriptional plant response to caterpillars. Interestingly, some important modulators of plant defense signalling, including WRKY transcription factor genes and ABA-dependent genes, were differentially induced in response to simultaneous aphid feeding at low or high density compared with responses to P. xylostella caterpillars feeding alone. Furthermore, aphids affected the P. xylostella-induced transcriptomic response in a density-dependent manner, which caused an acceleration in plant response against dual insect attack at high aphid density compared to dual insect attack at low aphid density. In conclusion, our study provides evidence that aphids influence the caterpillar-induced transcriptional response of A. thaliana in a density-dependent manner. It highlights the importance of addressing insect density to understand how plant responses to single attackers interfere with responses to other attackers and thus underlines the importance of the dynamics of transcriptional plant responses to multiple herbivory.
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http://dx.doi.org/10.1007/s00442-016-3758-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5239811PMC
January 2017

Genetic architecture of plant stress resistance: multi-trait genome-wide association mapping.

New Phytol 2017 Feb 4;213(3):1346-1362. Epub 2016 Oct 4.

Wageningen University and Research Plant Breeding, Wageningen University and Research, PO Box 386, 6700 AJ, Wageningen, the Netherlands.

Plants are exposed to combinations of various biotic and abiotic stresses, but stress responses are usually investigated for single stresses only. Here, we investigated the genetic architecture underlying plant responses to 11 single stresses and several of their combinations by phenotyping 350 Arabidopsis thaliana accessions. A set of 214 000 single nucleotide polymorphisms (SNPs) was screened for marker-trait associations in genome-wide association (GWA) analyses using tailored multi-trait mixed models. Stress responses that share phytohormonal signaling pathways also share genetic architecture underlying these responses. After removing the effects of general robustness, for the 30 most significant SNPs, average quantitative trait locus (QTL) effect sizes were larger for dual stresses than for single stresses. Plants appear to deploy broad-spectrum defensive mechanisms influencing multiple traits in response to combined stresses. Association analyses identified QTLs with contrasting and with similar responses to biotic vs abiotic stresses, and below-ground vs above-ground stresses. Our approach allowed for an unprecedented comprehensive genetic analysis of how plants deal with a wide spectrum of stress conditions.
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http://dx.doi.org/10.1111/nph.14220DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5248600PMC
February 2017

Novel Genes Affecting the Interaction between the Cabbage Whitefly and Arabidopsis Uncovered by Genome-Wide Association Mapping.

PLoS One 2015 23;10(12):e0145124. Epub 2015 Dec 23.

Wageningen UR Plant Breeding, Wageningen University, Wageningen, The Netherlands.

Plants have evolved a variety of ways to defend themselves against biotic attackers. This has resulted in the presence of substantial variation in defense mechanisms among plants, even within a species. Genome-wide association (GWA) mapping is a useful tool to study the genetic architecture of traits, but has so far only had limited exploitation in studies of plant defense. Here, we study the genetic architecture of defense against the phloem-feeding insect cabbage whitefly (Aleyrodes proletella) in Arabidopsis thaliana. We determined whitefly performance, i.e. the survival and reproduction of whitefly females, on 360 worldwide selected natural accessions and subsequently performed GWA mapping using 214,051 SNPs. Substantial variation for whitefly adult survival and oviposition rate (number of eggs laid per female per day) was observed between the accessions. We identified 39 candidate SNPs for either whitefly adult survival or oviposition rate, all with relatively small effects, underpinning the complex architecture of defense traits. Among the corresponding candidate genes, i.e. genes in linkage disequilibrium (LD) with candidate SNPs, none have previously been identified as a gene playing a role in the interaction between plants and phloem-feeding insects. Whitefly performance on knock-out mutants of a number of candidate genes was significantly affected, validating the potential of GWA mapping for novel gene discovery in plant-insect interactions. Our results show that GWA analysis is a very useful tool to gain insight into the genetic architecture of plant defense against herbivorous insects, i.e. we identified and validated several genes affecting whitefly performance that have not previously been related to plant defense against herbivorous insects.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0145124PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4689410PMC
July 2016

Quantitative resistance against Bemisia tabaci in Solanum pennellii: Genetics and metabolomics.

J Integr Plant Biol 2016 Apr 19;58(4):397-412. Epub 2016 Jan 19.

Wageningen UR Plant Breeding, Wageningen University and Research Centre, P.O. Box 386, 6700AJ, Wageningen, The Netherlands.

The whitefly Bemisia tabaci is a serious threat in tomato cultivation worldwide as all varieties grown today are highly susceptible to this devastating herbivorous insect. Many accessions of the tomato wild relative Solanum pennellii show a high resistance towards B. tabaci. A mapping approach was used to elucidate the genetic background of whitefly-resistance related traits and associated biochemical traits in this species. Minor quantitative trait loci (QTLs) for whitefly adult survival (AS) and oviposition rate (OR) were identified and some were confirmed in an F2 BC1 population, where they showed increased percentages of explained variance (more than 30%). Bulked segregant analyses on pools of whitefly-resistant and -susceptible F2 plants enabled the identification of metabolites that correlate either with resistance or susceptibility. Genetic mapping of these metabolites showed that a large number of them co-localize with whitefly-resistance QTLs. Some of these whitefly-resistance QTLs are hotspots for metabolite QTLs. Although a large number of metabolite QTLs correlated to whitefly resistance or susceptibility, most of them are yet unknown compounds and further studies are needed to identify the metabolic pathways and genes involved. The results indicate a direct genetic correlation between biochemical-based resistance characteristics and reduced whitefly incidence in S. pennellii.
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http://dx.doi.org/10.1111/jipb.12449DOI Listing
April 2016

Ethylene: Traffic Controller on Hormonal Crossroads to Defense.

Plant Physiol 2015 Dec 19;169(4):2371-9. Epub 2015 Oct 19.

Plant-Microbe Interactions, Department of Biology, Faculty of Science, Utrecht University, 3508 TB Utrecht, The Netherlands.

Ethylene (ET) is an important hormone in plant responses to microbial pathogens and herbivorous insects, and in the interaction of plants with beneficial microbes and insects. Early ET signaling events during these biotic interactions involve activities of mitogen-activated protein kinases and ETHYLENE RESPONSE FACTOR transcription factors. Rather than being the principal regulator, ET often modulates defense signaling pathways, including those regulated by jasmonic acid and salicylic acid. Hormonal signal integrations with ET steer the defense signaling network to activate specific defenses that can have direct effects on attackers, or systemically prime distant plant parts for enhanced defense against future attack. ET also regulates volatile signals that attract carnivorous enemies of herbivores or warn neighboring plants. Conversely, ET signaling can also be exploited by attackers to hijack the defense signaling network to suppress effective defenses. In this review, we summarize recent findings on the significant role of ET in the plants' battle against their enemies.
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http://dx.doi.org/10.1104/pp.15.01020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4677896PMC
December 2015

Parasitism overrides herbivore identity allowing hyperparasitoids to locate their parasitoid host using herbivore-induced plant volatiles.

Mol Ecol 2015 Jun 6;24(11):2886-99. Epub 2015 May 6.

Laboratory of Entomology, Wageningen University, Wageningen, The Netherlands.

Foraging success of predators profoundly depends on reliable and detectable cues indicating the presence of their often inconspicuous prey. Carnivorous insects rely on chemical cues to optimize foraging efficiency. Hyperparasitoids that lay their eggs in the larvae or pupae of parasitic wasps may find their parasitoid hosts developing in different herbivores. They can use herbivore-induced plant volatiles (HIPVs) to locate parasitized caterpillars. Because different herbivore species induce different HIPV emission from plants, hyperparasitoids may have to deal with large variation in volatile information that indicates host presence. In this study, we used an ecogenomics approach to first address whether parasitized caterpillars of two herbivore species (Pieris rapae and P. brassicae) induce similar transcriptional and metabolomic responses in wild Brassica oleracea plants and, second, whether hyperparasitoids Lysibia nana are able to discriminate between these induced plant responses to locate their parasitoid host in different herbivores under both laboratory and field conditions. Our study revealed that both herbivore identity and parasitism affect plant transcriptional and metabolic responses to herbivory. We also found that hyperparasitoids are able to respond to HIPVs released by wild B. oleracea under both laboratory and field conditions. In addition, we observed stronger attraction of hyperparasitoids to HIPVs when plants were infested with parasitized caterpillars. However, hyperparasitoids were equally attracted to plants infested by either herbivore species. Our results indicate that parasitism plays a major role in HIPV-mediated plant-hyperparasitoid interactions. Furthermore, these findings also indicate that plant trait-mediated indirect interaction networks play important roles in community-wide species interactions.
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http://dx.doi.org/10.1111/mec.13164DOI Listing
June 2015

Constitutive overexpression of the pollen specific gene SKS13 in leaves reduces aphid performance on Arabidopsis thaliana.

BMC Plant Biol 2014 Aug 14;14:217. Epub 2014 Aug 14.

Background: Plants have developed a variety of mechanisms to counteract aphid attacks. They activate their defences by changing the expression of specific genes. Previously we identified an activation tag mutant of Arabidopsis thaliana on which Myzus persicae population development was reduced. Activation tag mutants are gain-of-function in which the expression of a gene is increased by the insertion of the Cauliflower mosaic virus 35S enhancer that acts on the natural promoter. By further characterizing this previously identified mutant we identified a gene that reduces performance of M. persicae and also provided clues about the mechanism involved.

Results: We show that SKU5 SIMILAR 13 (SKS13), a gene whose expression in wild type plants is restricted to pollen and non-responsive to M. persicae attack, is overexpressed in the A. thaliana mutant showing reduced performance of M. persicae. Monitoring M. persicae feeding behaviour on SKS13 overexpressing plants indicated that M. persicae have difficulties feeding from the phloem. The constitutive expression of SKS13 results in accumulation of reactive oxygen species, which is possibly regulated through the jasmonic acid pathway. The enhanced resistance is not aphid species specific as also the population development of Brevicoryne brassicae was affected.

Conclusions: We demonstrate that constitutive expression in leaves of the pollen-specific gene SKS13 can enhance plant defence, resulting in a reduction of M. persicae population development and also decreases the transmission of persistent viruses. Overexpression of SKS13 in A. thaliana also affects B. brassicae and possibly other phloem feeding insects as well. Identifying genes that can enhance plant defence against insects will be important to open up new avenues for the development of insect resistant crop plants.
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http://dx.doi.org/10.1186/s12870-014-0217-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4243735PMC
August 2014

Synergistic effects of direct and indirect defences on herbivore egg survival in a wild crucifer.

Proc Biol Sci 2014 Aug;281(1789):20141254

Resource Ecology Group, Wageningen University, Droevendaalsesteeg 3a, 6708 PB Wageningen, The Netherlands.

Evolutionary theory of plant defences against herbivores predicts a trade-off between direct (anti-herbivore traits) and indirect defences (attraction of carnivores) when carnivore fitness is reduced. Such a trade-off is expected in plant species that kill herbivore eggs by exhibiting a hypersensitive response (HR)-like necrosis, which should then negatively affect carnivores. We used the black mustard (Brassica nigra) to investigate how this potentially lethal direct trait affects preferences and/or performances of specialist cabbage white butterflies (Pieris spp.), and their natural enemies, tiny egg parasitoid wasps (Trichogramma spp.). Both within and between black mustard populations, we observed variation in the expression of Pieris egg-induced HR. Butterfly eggs on plants with HR-like necrosis suffered lower hatching rates and higher parasitism than eggs that did not induce the trait. In addition, Trichogramma wasps were attracted to volatiles of egg-induced plants that also expressed HR, and this attraction depended on the Trichogramma strain used. Consequently, HR did not have a negative effect on egg parasitoid survival. We conclude that even within a system where plants deploy lethal direct defences, such defences may still act with indirect defences in a synergistic manner to reduce herbivore pressure.
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http://dx.doi.org/10.1098/rspb.2014.1254DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4100524PMC
August 2014

Overexpression of IRM1 enhances resistance to aphids in Arabidopsis thaliana.

PLoS One 2013 12;8(8):e70914. Epub 2013 Aug 12.

Wageningen UR Plant Breeding, Wageningen University, Wageningen, The Netherlands.

Aphids are insects that cause direct damage to crops by the removal of phloem sap, but more importantly they spread devastating viruses. Aphids use their sophisticated mouthpart (i.e. stylet) to feed from the phloem sieve elements of the host plant. To identify genes that affect host plant resistance to aphids, we previously screened an Arabidopsis thaliana activation tag mutant collection. In such mutants, tagged genes are overexpressed by a strong 35S enhancer adjacent to the natural promoter, resulting in a dominant gain-of-function phenotype. We previously identified several of these mutants on which the aphid Myzus persicae showed a reduced population development compared with wild type. In the present study we show that the gene responsible for the phenotype of one of the mutants is At5g65040 and named this gene Increased Resistance to Myzus persicae 1 (IRM1). Overexpression of the cloned IRM1 gene conferred a phenotype identical to that of the original mutant. Conversely, an IRM1 knockout mutant promoted aphid population development compared to the wild type. We performed Electrical Penetration Graph analysis to investigate how probing and feeding behaviour of aphids was affected on plants that either overexpressed IRM1 or contained a knockout mutation in this gene. The EPG results indicated that the aphids encounter resistance factors while reaching for the phloem on the overexpressing line. This resistance mechanism also affected other aphid species and is suggested to be of mechanical nature. Interestingly, genetic variation for IRM1 expression in response to aphid attack was observed. Upon aphid attack the expression of IRM1 was initially (after 6 hours) induced in ecotype Wassilewskija followed by suppression. In Columbia-0, IRM1 expression was already suppressed six hours after the start of the infestation. The resistance conferred by the overexpression of IRM1 in A. thaliana trades off with plant growth.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0070914PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3741364PMC
March 2014

Jasmonate and ethylene signaling mediate whitefly-induced interference with indirect plant defense in Arabidopsis thaliana.

New Phytol 2013 Mar 11;197(4):1291-1299. Epub 2013 Jan 11.

Laboratory of Entomology, Wageningen University, PO Box 8031, 6700 EH, Wageningen, the Netherlands.

Upon herbivore attack, plants activate an indirect defense, that is, the release of a complex mixture of volatiles that attract natural enemies of the herbivore. When plants are simultaneously exposed to two herbivore species belonging to different feeding guilds, one herbivore may interfere with the indirect plant defense induced by the other herbivore. However, little is understood about the mechanisms underlying such interference. Here, we address the effect of herbivory by the phloem-feeding whitefly Bemisia tabaci on the induced indirect defense of Arabidopsis thaliana plants to Plutella xylostella caterpillars, that is, the attraction of the parasitoid wasp Diadegma semiclausum. Assays with various Arabidopsis mutants reveal that B. tabaci infestation interferes with indirect plant defense induced by P. xylostella, and that intact jasmonic acid and ethylene signaling are required for such interference caused by B. tabaci. Chemical analysis of plant volatiles showed that the composition of the blend emitted in response to the caterpillars was significantly altered by co-infestation with whiteflies. Moreover, whitefly infestation also had a considerable effect on the transcriptomic response of the plant to the caterpillars. Understanding the mechanisms underlying a plant's responses to multiple attackers will be important for the development of crop protection strategies in a multi-attacker context.
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http://dx.doi.org/10.1111/nph.12106DOI Listing
March 2013

High throughput phenotyping for aphid resistance in large plant collections.

Plant Methods 2012 Aug 17;8(1):33. Epub 2012 Aug 17.

Wageningen UR, Plant Breeding, PO, Box 386, 6700, AJ, Wageningen, the Netherlands.

Background: Phloem-feeding insects are among the most devastating pests worldwide. They not only cause damage by feeding from the phloem, thereby depleting the plant from photo-assimilates, but also by vectoring viruses. Until now, the main way to prevent such problems is the frequent use of insecticides. Applying resistant varieties would be a more environmental friendly and sustainable solution. For this, resistant sources need to be identified first. Up to now there were no methods suitable for high throughput phenotyping of plant germplasm to identify sources of resistance towards phloem-feeding insects.

Results: In this paper we present a high throughput screening system to identify plants with an increased resistance against aphids. Its versatility is demonstrated using an Arabidopsis thaliana activation tag mutant line collection. This system consists of the green peach aphid Myzus persicae (Sulzer) and the circulative virus Turnip yellows virus (TuYV). In an initial screening, with one plant representing one mutant line, 13 virus-free mutant lines were identified by ELISA. Using seeds produced from these lines, the putative candidates were re-evaluated and characterized, resulting in nine lines with increased resistance towards the aphid.

Conclusions: This M. persicae-TuYV screening system is an efficient, reliable and quick procedure to identify among thousands of mutated lines those resistant to aphids. In our study, nine mutant lines with increased resistance against the aphid were selected among 5160 mutant lines in just 5 months by one person. The system can be extended to other phloem-feeding insects and circulative viruses to identify insect resistant sources from several collections, including for example genebanks and artificially prepared mutant collections.
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http://dx.doi.org/10.1186/1746-4811-8-33DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3489598PMC
August 2012

Exploiting natural variation to identify insect-resistance genes.

Plant Biotechnol J 2011 Oct 16;9(8):819-25. Epub 2011 Jun 16.

Wageningen UR Plant Breeding, Wageningen University & Research Centre, Wageningen, The Netherlands.

Herbivorous insects are widespread and often serious constraints to crop production. The use of insect-resistant crops is a very effective way to control insect pests in agriculture, and the development of such crops can be greatly enhanced by knowledge on plant resistance mechanisms and the genes involved. Plants have evolved diverse ways to cope with insect attack that has resulted in natural variation for resistance towards herbivorous insects. Studying the molecular genetics and transcriptional background of this variation has facilitated the identification of resistance genes and processes that lead to resistance against insects. With the development of new technologies, molecular studies are not restricted to model plants anymore. This review addresses the need to exploit natural variation in resistance towards insects to increase our knowledge on resistance mechanisms and the genes involved. We will discuss how this knowledge can be exploited in breeding programmes to provide sustainable crop protection against insect pests. Additionally, we discuss the current status of genetic research on insect-resistance genes. We conclude that insect-resistance mechanisms are still unclear at the molecular level and that exploiting natural variation with novel technologies will contribute greatly to the development of insect-resistant crop varieties.
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http://dx.doi.org/10.1111/j.1467-7652.2011.00635.xDOI Listing
October 2011

Natural variation in herbivore-induced volatiles in Arabidopsis thaliana.

J Exp Bot 2010 Jun 20;61(11):3041-56. Epub 2010 May 20.

Laboratory of Entomology, Wageningen University, EH Wageningen, The Netherlands.

To study whether natural variation in Arabidopsis thaliana could be used to dissect the genetic basis of responses to herbivory in terms of induced volatile emissions, nine accessions were characterized upon herbivory by biting-chewing Pieris rapae caterpillars or after treatment with the phytohormone jasmonic acid (JA). Analysis of 73 compounds in the headspace showed quantitative differences in the emission rates of several individual compounds among the accessions. Moreover, variation in the emission of volatile compounds after JA treatment was reflected in the behaviour of the parasitoid Diadegma semiclausum when they were offered the headspace volatiles of several combinations of accessions in two-choice experiments. Accessions also differ in transcript levels of genes that are associated with the emission of plant volatiles. The genes BSMT1 and Cyp72A13 could be connected to the emission of methyl salicylate and (E,E)-4,8,12-trimethyltrideca-1,3,7,11-tetraene (TMTT), respectively. Overall, Arabidopsis showed interesting phenotypic variations with respect to the volatile blend emitted in response to herbivory that can be exploited to identify genes and alleles that underlie this important plant trait.
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http://dx.doi.org/10.1093/jxb/erq127DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2892144PMC
June 2010

Intraspecific variation in herbivore community composition and transcriptional profiles in field-grown Brassica oleracea cultivars.

J Exp Bot 2010 Mar 24;61(3):807-19. Epub 2009 Nov 24.

Plant Research International BV, Wageningen University and Research Centre, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands.

Intraspecific differences in plant defence traits are often correlated with variation in transcriptional profiles and can affect the composition of herbivore communities on field-grown plants. However, most studies on transcriptional profiling of plant-herbivore interactions have been carried out under controlled conditions in the laboratory or greenhouse and only a few examine intraspecific transcriptional variation. Here, intraspecific variation in herbivore community composition and transcriptional profiles between two Brassica oleracea cultivars grown in the field is addressed. Early in the season, no differences in community composition were found for naturally occurring herbivores, whereas cultivars differed greatly in abundance, species richness, and herbivore community later in the season. Genome-wide transcriptomic analysis using an Arabidopsis thaliana oligonucleotide microarray showed clear differences for the expression levels of 26 genes between the two cultivars later in the season. Several defence-related genes showed higher levels of expression in the cultivar that harboured the lowest numbers of herbivores. Our study shows that herbivore community composition develops differentially throughout the season on the two B. oleracea cultivars grown in the field. The correlation between the differences in herbivore communities and differential expression of particular defence-related genes is discussed.
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http://dx.doi.org/10.1093/jxb/erp347DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2814112PMC
March 2010

Responses of Brassica oleracea cultivars to infestation by the aphid Brevicoryne brassicae: an ecological and molecular approach.

Plant Cell Environ 2008 Nov 19;31(11):1592-605. Epub 2008 Aug 19.

Plant Research International, Wageningen University and Research Centre, Wageningen, the Netherlands.

Intraspecific variation in resistance or susceptibility to herbivorous insects has been widely studied through bioassays. However, few studies have combined this with a full transcriptomic analysis. Here, we take such an approach to study the interaction between the aphid Brevicoryne brassicae and four white cabbage (Brassica oleracea var. capitata) cultivars. Both under glasshouse and field conditions, two of the cultivars clearly supported a faster aphid population development than the other two, indicating that aphid population development was largely independent of the environmental conditions. Genome-wide transcriptomic analysis using 70-mer oligonucleotide microarrays based on the Arabidopsis thaliana genome showed that only a small number of genes were differentially regulated, and that this regulation was highly cultivar specific. The temporal pattern in the expression behaviour of two B. brassicae-responsive genes in all four cultivars together with targeted studies employing A. thaliana knockout mutants revealed a possible role for a trypsin-and-protease inhibitor in defence against B. brassicae. Conversely, a xyloglucan endotransglucosylase seemed to have no effect on aphid performance. Overall, this study shows clear intraspecific variation in B. brassicae susceptibility among B. oleracea cultivars under glasshouse and field conditions that can be partly explained by certain differences in induced transcriptional changes.
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http://dx.doi.org/10.1111/j.1365-3040.2008.01871.xDOI Listing
November 2008

Male-derived butterfly anti-aphrodisiac mediates induced indirect plant defense.

Proc Natl Acad Sci U S A 2008 Jul 14;105(29):10033-8. Epub 2008 Jul 14.

Department of Plant Sciences, Laboratory of Entomology, Wageningen University, PO Box 8031, 6700 EH Wageningen, The Netherlands.

Plants can recruit parasitic wasps in response to egg deposition by herbivorous insects-a sophisticated indirect plant defense mechanism. Oviposition by the Large Cabbage White butterfly Pieris brassicae on Brussels sprout plants induces phytochemical changes that arrest the egg parasitoid Trichogramma brassicae. Here, we report the identification of an elicitor of such an oviposition-induced plant response. Eliciting activity was present in accessory gland secretions released by mated female butterflies during egg deposition. In contrast, gland secretions from virgin female butterflies were inactive. In the male ejaculate, P. brassicae females receive the anti-aphrodisiac benzyl cyanide (BC) that reduces the females' attractiveness for subsequent mating. We detected this pheromone in the accessory gland secretion released by mated female butterflies. When applied onto leaves, BC alone induced phytochemical changes that arrested females of the egg parasitoid. Microarray analyses revealed a similarity in induced plant responses that may explain the arrest of T. brassicae to egg-laden and BC-treated plants. Thus, a male-derived compound endangers the offspring of the butterfly by inducing plant defense. Recently, BC was shown to play a role in foraging behavior of T. brassicae, by acting as a cue to facilitate phoretic transport by mated female butterflies to oviposition sites. Our results suggest that the anti-aphrodisiac pheromone incurs fitness costs for the butterfly by both mediating phoretic behavior and inducing plant defense.
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http://dx.doi.org/10.1073/pnas.0707809105DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2481310PMC
July 2008

Early season herbivore differentially affects plant defence responses to subsequently colonizing herbivores and their abundance in the field.

Mol Ecol 2008 Jul 28;17(14):3352-65. Epub 2008 Jun 28.

Laboratory of Entomology, Wageningen University, PO Box 8031, 6700 EH Wageningen, The Netherlands.

Induction of plant defences by early season herbivores can mediate interspecific herbivore competition. We have investigated plant-mediated competition between three herbivorous insects through studies at different levels of biological integration. We have addressed (i) gene expression; (ii) insect behaviour and performance under laboratory conditions; and (iii) population dynamics under field conditions. We studied the expression of genes encoding a trypsin inhibitor and genes that are involved in glucosinolate biosynthesis in response to early season herbivory by Pieris rapae caterpillars in Brassica oleracea plants. Furthermore, we studied the interaction of these transcriptional responses with responses to secondary herbivory by the two specialist herbivores, P. rapae and Plutella xylostella, and the generalist Mamestra brassicae. P. rapae-induced responses strongly interacted with plant responses to secondary herbivory. Sequential feeding by specialist herbivores resulted in enhanced or similar expression levels of defence-related genes compared to primary herbivory by specialists. Secondary herbivory by the generalist M. brassicae resulted in lower gene expression levels than in response to primary herbivory by this generalist. Larval performance of both specialist and generalist herbivores was negatively affected by P. rapae-induced plant responses. However, in the field the specialist P. xylostella was more abundant on P. rapae-induced plants and preferred these plants over undamaged plants in oviposition experiments. In contrast, the generalist M. brassicae was more abundant on control plants and preferred undamaged plants for oviposition. P. rapae did not discriminate between plants damaged by conspecifics or undamaged plants. Our study shows that early season herbivory differentially affects transcriptional responses involved in plant defence to secondary herbivores and their population development dependent upon their degree of host plant specialization.
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http://dx.doi.org/10.1111/j.1365-294X.2008.03838.xDOI Listing
July 2008

Genotypic variation in genome-wide transcription profiles induced by insect feeding: Brassica oleracea--Pieris rapae interactions.

BMC Genomics 2007 Jul 17;8:239. Epub 2007 Jul 17.

Plant Research International B.V., Wageningen University and Research Centre, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands.

Background: Transcriptional profiling after herbivore attack reveals, at the molecular level, how plants respond to this type of biotic stress. Comparing herbivore-induced transcriptional responses of plants with different phenotypes provides insight into plant defense mechanisms. Here, we compare the global gene expression patterns induced by Pieris rapae caterpillar attack in two white cabbage (Brassica oleracea var. capitata) cultivars. The two cultivars are shown to differ in their level of direct defense against caterpillar feeding. Because Brassica full genome microarrays are not yet available, 70-mer oligonucleotide microarrays based on the Arabidopsis thaliana genome were used for this non-model plant.

Results: The transcriptional responses of the two cultivars differed in timing as characterized by changes in their expression pattern after 24, 48 and 72 hours of caterpillar feeding. In addition, they also differed qualitatively. Surprisingly, of all genes induced at any time point, only one third was induced in both cultivars. Analyses of transcriptional responses after jasmonate treatment revealed that the difference in timing did not hold for the response to this phytohormone. Additionally, comparisons between Pieris rapae- and jasmonate-induced transcriptional responses showed that Pieris rapae induced more jasmonate-independent than jasmonate-dependent genes.

Conclusion: The present study clearly shows that global transcriptional responses in two cultivars of the same plant species in response to insect feeding can differ dramatically. Several of these differences involve genes that are known to have an impact on Pieris rapae performance and probably underlie different mechanisms of direct defense, present in the cultivars.
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http://dx.doi.org/10.1186/1471-2164-8-239DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1940009PMC
July 2007